Spatiotemporal Restriction of FUSCA3 Expression by Class I BPCs Promotes Ovule Development and Coordinates Embryo and Endosperm Growth

Abstract

Spatiotemporal regulation of gene expression plays an important role in developmental timing in plants and animals. FUSCA3 regulates the transition between different phases of development by acting as a link between different hormonal pathways in Arabidopsis.However, the mechanisms governing its spatiotemporal expression patterns are poorly understood. Here, we show that FUS3 is expressed in the chalaza and funiculus of the mature ovule and seed, but is repressed in the embryo sac, integuments and endosperm. FUS3 repression requires class I BASIC PENTACYSTEINE (BPC) proteins, which directly bind to the FUS3 locus and restrict its expression pattern. During vegetative and reproductive development, derepression of FUS3 in bpc1/2 or pML1:FUS3 misexpression lines results in dwarf plants carrying defective flowers and aborted ovules. Post-fertilization, ectopic FUS3 expression in the endosperm increases endosperm nuclei proliferation and seed size and delays or arrests embryo development. These phenotypes are rescued in bpc1/2 fus3-3. Lastly, class I BPCs interact with FIS-PRC2 (FERTILIZATION-INDEPENDENT SEED-Polycomb Repressive Complex 2), which represses FUS3 in the endosperm. We propose that BPC1/2 promotes the transition from reproductive to seed development by repressing FUS3 in ovule integuments. After fertilization, BPC1/2 and FIS-PRC2 repress FUS3 in the endosperm to coordinate endosperm and embryo growth.

Gibberellin-mediated RGA-LIKE1 degradation regulates embryo sac development in Arabidopsis

“…The phenotypes of the corresponding mutants demonstrate that these genes not only control integument identity but that they also play a role during megasporogenesis, since embryo sac maturation is impaired. Recently, it has been reported that the mis-expression of the transcription factor FUSCA3 in the integuments severely impairs embryo sac development ( Wu et al , 2020 ). Finally, ARGONAUTE5 ( AGO5 ), an effector of small RNA (sRNA) silencing pathways, is required to promote megagametogenesis in the FM ( Tucker et al , 2012 ).…”

Stop the FUSS: BPCs Restrict FUSCA3 Transcription to Promote Ovule and Seed Development

“…Moreover, the fus3-3 mutation partially rescued the stunted growth, aborted embryo, and arrested seed phenotypes of bpc1/2 double mutants. Collectively, Wu et al (2020) demonstrate that BPC proteins coordinate ovule and early seed development by recruiting PRC2 complexes that restrict FUS3 expression in key tissues and cell-types.…”

“…Previous research implicated BPCs in a wide range of developmental processes, as higher order bpc mutants exhibit ovule and seed abortion phenotypes (Monfared et al, 2011). Moreover, BPCs interact with PRC2 (POLYCOMB REPRESSOR COMPLEX2) subunits that were shown act at the FUS3 regions bound by class I BPCs (Xiao et al, 2017;Wu et al, 2020). To explore this further, the authors first confirmed that BPC1-3 interact with the PRC2 subunits FIS2 (FERTILIZATION INDEPENDENT SEED2) and MEDEA through yeast 2-hybrid and bimolecular fluorescence complementation assays.…”

Knowing When to Silence: Roles of Polycomb-Group Proteins in SAM Maintenance, Root Development, and Developmental Phase Transition

“…Before fertilization, the expression of FUS3 is restricted to the chalaza and funiculus of mature ovules. After fertilization, FUS3 is confined in the funiculus, seed coat, and chalaza [126]. BPC1 and 2 promote the transition from ovule to seed development by repressing FUS3 in ovule integuments.…”

“…The expression of genes encoding storage compounds in seeds, including CRUCIFERIN 3 (CRU3), CRUCIFERINA 1 (CRA1), Seed Storage Albumin 1 (SESA1), Seed Storage Albumin 2, (SESA2), Late Embryogenesis Abundant proteins (LEAs), and OLEOSINs (OLEOs), are also upregulated by fie mutation [87,106]. It has also been shown that BPC1 interacts with EMF2 and recruit EMF-PRC2 to the promoter of FUS3 to repress its expression during vegetative development [126].…”